Genomic insights into metabolic flux in hummingbirds
- Ariel Gershman1,2,
- Quinn Hauck1,
- Morag Dick3,4,
- Jerrica M. Jamison3,4,
- Michael Tassia5,
- Xabier Agirrezabala6,
- Saad Muhammad3,4,
- Raafay Ali3,4,
- Rachael E. Workman2,
- Mikel Valle6,
- G. William Wong7,
- Kenneth C. Welch Jr.3,4 and
- Winston Timp1,2
- 1Department of Biomedical Engineering, Johns Hopkins University, Baltimore, Maryland 21218, USA;
- 2Department of Molecular Biology and Genetics, Johns Hopkins University, Baltimore, Maryland 21287, USA;
- 3Cell & Systems Biology, University of Toronto, Toronto, Ontario M5S 3G5, Canada;
- 4Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, M1C 1A4, Canada;
- 5Department of Biology, Johns Hopkins University, Baltimore, Maryland 21218, USA;
- 6CIC bioGUNE, Basque Research and Technology Alliance (BRTA), 48160 Derio, Spain;
- 7Department of Physiology and Center for Metabolism and Obesity Research, School of Medicine, The Johns Hopkins University, Baltimore, Maryland 21205, USA
Abstract
Hummingbirds are very well adapted to sustain efficient and rapid metabolic shifts. They oxidize ingested nectar to directly fuel flight when foraging but have to switch to oxidizing stored lipids derived from ingested sugars during the night or long-distance migratory flights. Understanding how this organism moderates energy turnover is hampered by a lack of information regarding how relevant enzymes differ in sequence, expression, and regulation. To explore these questions, we generated a chromosome-scale genome assembly of the ruby-throated hummingbird (A. colubris) using a combination of long- and short-read sequencing, scaffolding it using existing assemblies. We then used hybrid long- and short-read RNA sequencing of liver and muscle tissue in fasted and fed metabolic states for a comprehensive transcriptome assembly and annotation. Our genomic and transcriptomic data found positive selection of key metabolic genes in nectivorous avian species and deletion of critical genes (SLC2A4, GCK) involved in glucostasis in other vertebrates. We found expression of a fructose-specific version of SLC2A5 putatively in place of insulin-sensitive SLC2A5, with predicted protein models suggesting affinity for both fructose and glucose. Alternative isoforms may even act to sequester fructose to preclude limitations from transport in metabolism. Finally, we identified differentially expressed genes from fasted and fed hummingbirds, suggesting key pathways for the rapid metabolic switch hummingbirds undergo.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.276779.122.
- Received March 21, 2022.
- Accepted April 26, 2023.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see https://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
